scholarly journals The economics of endosymbiotic gene transfer and the evolution of organellar genomes

Author(s):  
Steven Kelly

AbstractThe endosymbiosis of the bacterial progenitors of mitochondrion and the chloroplast are landmark events in the evolution of life on earth. While both organelles have retained substantial proteomic and biochemical complexity, this complexity is not reflected in the content of their genomes. Instead, the organellar genomes encode fewer than 5% of genes found in living relatives of their ancestors. While some of the 95% of missing organellar genes have been discarded, many have been transferred to the host nuclear genome through a process known as endosymbiotic gene transfer. Here we demonstrate that the energy liberated or consumed by a cell as a result of endosymbiotic gene transfer can be sufficient to provide a selectable advantage for retention or nuclear-transfer of organellar genes in eukaryotic cells. We further demonstrate that for realistic estimates of protein abundances, organellar protein import costs, host cell sizes, and cellular investment in organelles that it is energetically favourable to transfer the majority of organellar genes to the nuclear genome. Moreover, we show that the selective advantage of such transfers is sufficiently large to enable such events to rapidly reach fixation. Thus, endosymbiotic gene transfer can be advantageous in the absence of any additional benefit to the host cell, providing new insight into the processes that have shaped eukaryotic genome evolution.One sentence summaryThe high copy number of organellar genomes renders endosymbiotic gene transfer energetically favourable for the vast majority of organellar genes.

2021 ◽  
Vol 22 (1) ◽  
Author(s):  
Steven Kelly

Abstract Background The endosymbiosis of the bacterial progenitors of the mitochondrion and the chloroplast are landmark events in the evolution of life on Earth. While both organelles have retained substantial proteomic and biochemical complexity, this complexity is not reflected in the content of their genomes. Instead, the organellar genomes encode fewer than 5% of the genes found in living relatives of their ancestors. While many of the 95% of missing organellar genes have been discarded, others have been transferred to the host nuclear genome through a process known as endosymbiotic gene transfer. Results Here, we demonstrate that the difference in the per-cell copy number of the organellar and nuclear genomes presents an energetic incentive to the cell to either delete organellar genes or transfer them to the nuclear genome. We show that, for the majority of transferred organellar genes, the energy saved by nuclear transfer exceeds the costs incurred from importing the encoded protein into the organelle where it can provide its function. Finally, we show that the net energy saved by endosymbiotic gene transfer can constitute an appreciable proportion of total cellular energy budgets and is therefore sufficient to impart a selectable advantage to the cell. Conclusion Thus, reduced cellular cost and improved energy efficiency likely played a role in the reductive evolution of mitochondrial and chloroplast genomes and the transfer of organellar genes to the nuclear genome.


2017 ◽  
Vol 01 (02) ◽  
pp. 108-120 ◽  
Author(s):  
Nick Lane

All complex life on Earth is composed of ‘eukaryotic’ cells. Eukaryotes arose just once in 4 billion years, via an endosymbiosis — bacteria entered a simple host cell, evolving into mitochondria, the ‘powerhouses’ of complex cells. Mitochondria lost most of their genes, retaining only those needed for respiration, giving eukaryotes ‘multi-bacterial’ power without the costs of maintaining thousands of complete bacterial genomes. These energy savings supported a substantial expansion in nuclear genome size, and far more protein synthesis from each gene.


2014 ◽  
Vol 83 (4) ◽  
pp. 399-407 ◽  
Author(s):  
Przemysław Gagat ◽  
Paweł Mackiewicz

The rhizarian amoeba <em>Paulinella chromatophora</em> harbors two photosynthetic cyanobacterial endosymbionts (chromatophores), acquired independently of primary plastids of glaucophytes, red algae and green plants. These endosymbionts have lost many essential genes, and transferred substantial number of genes to the host nuclear genome via endosymbiotic gene transfer (EGT), including those involved in photosynthesis. This indicates that, similar to primary plastids, <em>Paulinella</em> endosymbionts must have evolved a transport system to import their EGT-derived proteins. This system involves vesicular trafficking to the outer chromatophore membrane and presumably a simplified Tic-like complex at the inner chromatophore membrane. Since both sequenced <em>Paulinella</em> strains have been shown to undergo differential plastid gene losses, they do not have to possess the same set of Toc and Tic homologs. We searched the genome of <em>Paulinella</em> FK01 strain for potential Toc and Tic homologs, and compared the results with the data obtained for <em>Paulinella</em> CCAC 0185 strain, and 72 cyanobacteria, eight Archaeplastida as well as some other bacteria. Our studies revealed that chromatophore genomes from both <em>Paulinella</em> strains encode the same set of translocons that could potentially create a simplified but fully-functional Tic-like complex at the inner chromatophore membranes. The common maintenance of the same set of translocon proteins in two <em>Paulinella</em> strains suggests a similar import mechanism and/or supports the proposed model of protein import. Moreover, we have discovered a new putative Tic component, Tic62, a redox sensor protein not identified in previous comparative studies of <em>Paulinella</em> translocons.


2009 ◽  
Vol 364 (1527) ◽  
pp. 2229-2239 ◽  
Author(s):  
Gregory P. Fournier ◽  
Jinling Huang ◽  
J. Peter Gogarten

Horizontal gene transfer (HGT) is often considered to be a source of error in phylogenetic reconstruction, causing individual gene trees within an organismal lineage to be incongruent, obfuscating the ‘true’ evolutionary history. However, when identified as such, HGTs between divergent organismal lineages are useful, phylogenetically informative characters that can provide insight into evolutionary history. Here, we discuss several distinct HGT events involving all three domains of life, illustrating the selective advantages that can be conveyed via HGT, and the utility of HGT in aiding phylogenetic reconstruction and in dating the relative sequence of speciation events. We also discuss the role of HGT from extinct lineages, and its impact on our understanding of the evolution of life on Earth. Organismal phylogeny needs to incorporate reticulations; a simple tree does not provide an accurate depiction of the processes that have shaped life's history.


2019 ◽  
Vol 19 (1) ◽  
Author(s):  
Nan Zhao ◽  
Corrinne E. Grover ◽  
Zhiwen Chen ◽  
Jonathan F. Wendel ◽  
Jinping Hua

Abstract Background Intergenomic gene transfer (IGT) between nuclear and organellar genomes is a common phenomenon during plant evolution. Gossypium is a useful model to evaluate the genomic consequences of IGT for both diploid and polyploid species. Here, we explore IGT among nuclear, mitochondrial, and plastid genomes of four cotton species, including two allopolyploids and their model diploid progenitors (genome donors, G. arboreum: A2 and G. raimondii: D5). Results Extensive IGT events exist for both diploid and allotetraploid cotton (Gossypium) species, with the nuclear genome being the predominant recipient of transferred DNA followed by the mitochondrial genome. The nuclear genome has integrated 100 times more foreign sequences than the mitochondrial genome has in total length. In the nucleus, the integrated length of chloroplast DNA (cpDNA) was between 1.87 times (in diploids) to nearly four times (in allopolyploids) greater than that of mitochondrial DNA (mtDNA). In the mitochondrion, the length of nuclear DNA (nuDNA) was typically three times than that of cpDNA. Gossypium mitochondrial genomes integrated three nuclear retrotransposons and eight chloroplast tRNA genes, and incorporated chloroplast DNA prior to divergence between the diploids and allopolyploid formation. For mitochondrial chloroplast-tRNA genes, there were 2-6 bp conserved microhomologies flanking their insertion sites across distantly related genera, which increased to 10 bp microhomologies for the four cotton species studied. For organellar DNA sequences, there are source hotspots, e.g., the atp6-trnW intergenic region in the mitochondrion and the inverted repeat region in the chloroplast. Organellar DNAs in the nucleus were rarely expressed, and at low levels. Surprisingly, there was asymmetry in the survivorship of ancestral insertions following allopolyploidy, with most numts (nuclear mitochondrial insertions) decaying or being lost whereas most nupts (nuclear plastidial insertions) were retained. Conclusions This study characterized and compared intracellular transfer among nuclear and organellar genomes within two cultivated allopolyploids and their ancestral diploid cotton species. A striking asymmetry in the fate of IGTs in allopolyploid cotton was discovered, with numts being preferentially lost relative to nupts. Our results connect intergenomic gene transfer with allotetraploidy and provide new insight into intracellular genome evolution.


Genes ◽  
2018 ◽  
Vol 9 (8) ◽  
pp. 412 ◽  
Author(s):  
Natalia Mallo ◽  
Justin Fellows ◽  
Carla Johnson ◽  
Lilach Sheiner

: The organelles of endosymbiotic origin, plastids, and mitochondria, evolved through the serial acquisition of endosymbionts by a host cell. These events were accompanied by gene transfer from the symbionts to the host, resulting in most of the organellar proteins being encoded in the cell nuclear genome and trafficked into the organelle via a series of translocation complexes. Much of what is known about organelle protein translocation mechanisms is based on studies performed in common model organisms; e.g., yeast and humans or Arabidopsis. However, studies performed in divergent organisms are gradually accumulating. These studies provide insights into universally conserved traits, while discovering traits that are specific to organisms or clades. Apicomplexan parasites feature two organelles of endosymbiotic origin: a secondary plastid named the apicoplast and a mitochondrion. In the context of the diseases caused by apicomplexan parasites, the essential roles and divergent features of both organelles make them prime targets for drug discovery. This potential and the amenability of the apicomplexan Toxoplasma gondii to genetic manipulation motivated research about the mechanisms controlling both organelles’ biogenesis. Here we provide an overview of what is known about apicomplexan organelle protein import. We focus on work done mainly in T. gondii and provide a comparison to model organisms.


2014 ◽  
Vol 57 (5) ◽  
pp. 897-902 ◽  
Author(s):  
AnHuai Lu ◽  
Xin Wang ◽  
Yan Li ◽  
HongRui Ding ◽  
ChangQiu Wang ◽  
...  

2021 ◽  
Vol 30 (5) ◽  
pp. 497-520
Author(s):  
Zdravka Kostova ◽  

The article discusses successive stages in the evolution of life up to the establishment of the prokaryotic cell emphasizing the transitions from pre-biotic environment to organic precursors, pre-RNA-RNA, RNA-proteins-DNA, DNA-LUCA. They are paired with the development of pre-biotic structural progenitors of a cell - micelles, vesicles, protocells, prokaryotic ancestor, two prokaryotic branches – Eubacteria and Archaebacteria. The driving force is the natural selection (chemical, biochemical and biological), maintaining the correspondence between the emerging structures and their environment.


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